Login Register Cart 0
Mini-Review Article

Intracellular Compartmentalization: A Key Determinant of MicroRNA Functions

Author(s): Rohit Nalavade* and Mohini Singh*

Volume 12, Issue 2, 2023

Published on: 19 April, 2023

Page: [114 - 130] Pages: 17

DOI: 10.2174/2211536612666230330184006

Price: $65

Open Access Journals Promotions 2
Abstract

Being an integral part of the eukaryotic transcriptome, miRNAs are regarded as vital regulators of diverse developmental and physiological processes. Clearly, miRNA activity is kept in check by various regulatory mechanisms that control their biogenesis and decay pathways. With the increasing technical depth of RNA profiling technologies, novel insights have unravelled the spatial diversity exhibited by miRNAs inside a cell. Compartmentalization of miRNAs adds complexity to the regulatory circuits of miRNA expression, thereby providing superior control over the miRNA function. This review provides a bird’s eye view of miRNAs expressed in different subcellular locations, thus affecting the gene regulatory pathways therein. Occurrence of miRNAs in diverse intracellular locales also reveals various unconventional roles played by miRNAs in different cellular organelles and expands the scope of miRNA functions beyond their traditionally known repressive activities.

Keywords: Eukaryotic transcriptome, biogenesis, prominent roles, endogenously or exogenously, miRNAs, gene regulatory pathways.

Next »
Graphical Abstract

[1]
Bartel DP. MicroRNAs: Target recognition and regulatory functions. Cell 2009; 136(2): 215-33.
[http://dx.doi.org/10.1016/j.cell.2009.01.002] [PMID: 19167326]
[2]
Kozomara A, Birgaoanu M, Griffiths-Jones S. miRBase: From microRNA sequences to function. Nucleic Acids Res 2019; 47(D1): D155-62.
[http://dx.doi.org/10.1093/nar/gky1141] [PMID: 30423142]
[3]
Chi SW, Zang JB, Mele A, Darnell RB. Argonaute HITS-CLIP decodes microRNA–mRNA interaction maps. Nature 2009; 460(7254): 479-86.
[http://dx.doi.org/10.1038/nature08170] [PMID: 19536157]
[4]
Hafner M, Landthaler M, Burger L, et al. Transcriptome-wide identification of RNA-binding protein and microRNA target sites by PAR-CLIP. Cell 2010; 141(1): 129-41.
[http://dx.doi.org/10.1016/j.cell.2010.03.009] [PMID: 20371350]
[5]
Hanna J, Hossain GS, Kocerha J. The potential for microRNA therapeutics and clinical research. Front Genet 2019; 10: 478.
[http://dx.doi.org/10.3389/fgene.2019.00478] [PMID: 31156715]
[6]
Klein U, Lia M, Crespo M, et al. The DLEU2/miR-15a/16-1 cluster controls B cell proliferation and its deletion leads to chronic lymphocytic leukemia. Cancer Cell 2010; 17(1): 28-40.
[http://dx.doi.org/10.1016/j.ccr.2009.11.019] [PMID: 20060366]
[7]
Calin GA, Cimmino A, Fabbri M, et al. MiR-15a and miR-16-1 cluster functions in human leukemia. Proc Natl Acad Sci 2008; 105(13): 5166-71.
[http://dx.doi.org/10.1073/pnas.0800121105] [PMID: 18362358]
[8]
Bartel DP. Metazoan MicroRNAs. Cell 2018; 173(1): 20-51.
[http://dx.doi.org/10.1016/j.cell.2018.03.006] [PMID: 29570994]
[9]
Lu J, Getz G, Miska EA, et al. MicroRNA expression profiles classify human cancers. Nature 2005; 435(7043): 834-8.
[http://dx.doi.org/10.1038/nature03702] [PMID: 15944708]
[10]
Rüegger S, Großhans H. MicroRNA turnover: When, how, and why. Trends Biochem Sci 2012; 37(10): 436-46.
[http://dx.doi.org/10.1016/j.tibs.2012.07.002] [PMID: 22921610]
[11]
Gebert LFR, MacRae IJ. Regulation of microRNA function in animals. Nat Rev Mol Cell Biol 2019; 20(1): 21-37.
[http://dx.doi.org/10.1038/s41580-018-0045-7] [PMID: 30108335]
[12]
Chatterjee S, Fasler M, Büssing I, Großhans H. Target-mediated protection of endogenous microRNAs in C. elegans. Dev Cell 2011; 20(3): 388-96.
[http://dx.doi.org/10.1016/j.devcel.2011.02.008] [PMID: 21397849]
[13]
Ghini F, Rubolino C, Climent M, Simeone I, Marzi MJ, Nicassio F. Endogenous transcripts control miRNA levels and activity in mammalian cells by target-directed miRNA degradation. Nat Commun 2018; 9(1): 3119.
[http://dx.doi.org/10.1038/s41467-018-05182-9] [PMID: 30087332]
[14]
Kim YK, Heo I, Kim VN. Modifications of small RNAs and their associated proteins. Cell 2010; 143(5): 703-9.
[http://dx.doi.org/10.1016/j.cell.2010.11.018] [PMID: 21111232]
[15]
Kai ZS, Pasquinelli AE. MicroRNA assassins: factors that regulate the disappearance of miRNAs. Nat Struct Mol Biol 2010; 17(1): 5-10.
[http://dx.doi.org/10.1038/nsmb.1762] [PMID: 20051982]
[16]
Biemar F, Zinzen R, Ronshaugen M, Sementchenko V, Manak JR, Levine MS. Spatial regulation of microRNA gene expression in the Drosophila embryo. Proc Natl Acad Sci 2005; 102(44): 15907-11.
[http://dx.doi.org/10.1073/pnas.0507817102] [PMID: 16249329]
[17]
Pasquinelli AE, Reinhart BJ, Slack F, et al. Conservation of the sequence and temporal expression of let-7 heterochronic regulatory RNA. Nature 2000; 408(6808): 86-9.
[http://dx.doi.org/10.1038/35040556] [PMID: 11081512]
[18]
Rybak A, Fuchs H, Hadian K, et al. The let-7 target gene mouse lin-41 is a stem cell specific E3 ubiquitin ligase for the miRNA pathway protein Ago2. Nat Cell Biol 2009; 11(12): 1411-20.
[http://dx.doi.org/10.1038/ncb1987] [PMID: 19898466]
[19]
Wang J, Czech B, Crunk A, et al. Deep small RNA sequencing from the nematode Ascaris reveals conservation, functional diversification, and novel developmental profiles. Genome Res 2011; 21(9): 1462-77.
[http://dx.doi.org/10.1101/gr.121426.111] [PMID: 21685128]
[20]
Martinez NJ, Ow MC, Reece-Hoyes JS, Barrasa MI, Ambros VR, Walhout AJM. Genome-scale spatiotemporal analysis of Caenorhabditis elegans microRNA promoter activity. Genome Res 2008; 18(12): 2005-15.
[http://dx.doi.org/10.1101/gr.083055.108] [PMID: 18981266]
[21]
Lee EJ, Baek M, Gusev Y, Brackett DJ, Nuovo GJ, Schmittgen TD. Systematic evaluation of microRNA processing patterns in tissues, cell lines, and tumors. RNA 2008; 14(1): 35-42.
[http://dx.doi.org/10.1261/rna.804508] [PMID: 18025253]
[22]
Newman MA, Thomson JM, Hammond SM. Lin-28 interaction with the Let-7 precursor loop mediates regulated microRNA processing. RNA 2008; 14(8): 1539-49.
[http://dx.doi.org/10.1261/rna.1155108] [PMID: 18566191]
[23]
Ninova M, Ronshaugen M, Griffiths-Jones S. Conserved temporal patterns of microRNA expression in Drosophila support a developmental hourglass model. Genome Biol Evol 2014; 6(9): 2459-67.
[http://dx.doi.org/10.1093/gbe/evu183] [PMID: 25169982]
[24]
Landgraf P, Rusu M, Sheridan R, et al. A mammalian microRNA expression atlas based on small RNA library sequencing. Cell 2007; 129(7): 1401-14.
[http://dx.doi.org/10.1016/j.cell.2007.04.040] [PMID: 17604727]
[25]
Hinton A, Hunter SE, Afrikanova I, et al. sRNA-seq analysis of human embryonic stem cells and definitive endoderm reveals differentially expressed microRNAs and novel IsomiRs with distinct targets. Stem Cells 2014; 32(9): 2360-72.
[http://dx.doi.org/10.1002/stem.1739] [PMID: 24805944]
[26]
Lim LP, Lau NC, Garrett-Engele P, et al. Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 2005; 433(7027): 769-73.
[http://dx.doi.org/10.1038/nature03315] [PMID: 15685193]
[27]
Trabucchi M, Briata P, Garcia-Mayoral M, et al. The RNA-binding protein KSRP promotes the biogenesis of a subset of microRNAs. Nature 2009; 459(7249): 1010-4.
[http://dx.doi.org/10.1038/nature08025] [PMID: 19458619]
[28]
Park JE, Heo I, Tian Y, et al. Dicer recognizes the 5′ end of RNA for efficient and accurate processing. Nature 2011; 475(7355): 201-5.
[http://dx.doi.org/10.1038/nature10198] [PMID: 21753850]
[29]
Zeng Y, Cullen BR. RNA interference in human cells is restricted to the cytoplasm. RNA 2002; 8(7): 855-60.
[http://dx.doi.org/10.1017/S1355838202020071] [PMID: 12166640]
[30]
Bernstein E, Caudy AA, Hammond SM, Hannon GJ. Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 2001; 409(6818): 363-6.
[http://dx.doi.org/10.1038/35053110] [PMID: 11201747]
[31]
MacRae IJ, Zhou K, Li F, et al. Structural basis for double-stranded RNA processing by Dicer. Science 2006; 311(5758): 195-8.
[http://dx.doi.org/10.1126/science.1121638]
[32]
Gregory RI, Chendrimada TP, Cooch N, Shiekhattar R. Human RISC couples microRNA biogenesis and posttranscriptional gene silencing. Cell 2005; 123(4): 631-40.
[http://dx.doi.org/10.1016/j.cell.2005.10.022] [PMID: 16271387]
[33]
Matranga C, Tomari Y, Shin C, Bartel DP, Zamore PD. Passenger-strand cleavage facilitates assembly of siRNA into Ago2-containing RNAi enzyme complexes. Cell 2005; 123(4): 607-20.
[http://dx.doi.org/10.1016/j.cell.2005.08.044] [PMID: 16271386]
[34]
Pillai RS, Bhattacharyya SN, Artus CG, et al. Molecular biology: Inhibition of translational initiation by let-7 microRNA in human cells. Science 2005; 309(5740): 1573-6.
[35]
Humphreys DT, Westman BJ, Martin DIK, Preiss T. MicroRNAs control translation initiation by inhibiting eukaryotic initiation factor 4E/cap and poly(A) tail function. Proc Natl Acad Sci 2005; 102(47): 16961-6.
[http://dx.doi.org/10.1073/pnas.0506482102] [PMID: 16287976]
[36]
Liu J, Valencia-Sanchez MA, Hannon GJ, Parker R. MicroRNA-dependent localization of targeted mRNAs to mammalian P-bodies. Nat Cell Biol 2005; 7(7): 719-23.
[http://dx.doi.org/10.1038/ncb1274] [PMID: 15937477]
[37]
Eulalio A, Behm-Ansmant I, Schweizer D, Izaurralde E. P-body formation is a consequence, not the cause, of RNA-mediated gene silencing. Mol Cell Biol 2007; 27(11): 3970-81.
[http://dx.doi.org/10.1128/MCB.00128-07] [PMID: 17403906]
[38]
Chu C, Rana TM. Translation repression in human cells by microRNA-induced gene silencing requires RCK/p54. PLoS Biol 2006; 4(7): e210.
[http://dx.doi.org/10.1371/journal.pbio.0040210] [PMID: 16756390]
[39]
Sheth U, Parker R. Decapping and decay of messenger RNA occur in cytoplasmic processing bodies. Science 2003; 300(5620): 805-8.
[http://dx.doi.org/10.1126/science.1082320]
[40]
Bhattacharyya SN, Habermacher R, Martine U, Closs EI, Filipowicz W. Relief of microRNA-mediated translational repression in human cells subjected to stress. Cell 2006; 125(6): 1111-24.
[http://dx.doi.org/10.1016/j.cell.2006.04.031] [PMID: 16777601]
[41]
Stalder L, Heusermann W, Sokol L, et al. The rough endoplasmatic reticulum is a central nucleation site of siRNA-mediated RNA silencing. EMBO J 2013; 32(8): 1115-27.
[http://dx.doi.org/10.1038/emboj.2013.52] [PMID: 23511973]
[42]
Barman B, Bhattacharyya SN. mRNA targeting to endoplasmic reticulum precedes AGO protein interaction and MicroRNA (miRNA)-mediated translation repression in mammalian cells. J Biol Chem 2015; 290(41): 24650-6.
[http://dx.doi.org/10.1074/jbc.C115.661868] [PMID: 26304123]
[43]
Upton JP, Wang L, Han D, et al. IRE1α cleaves select microRNAs during ER stress to derepress translation of proapoptotic Caspase-2. Science 2012; 338(6108): 818-22.
[http://dx.doi.org/10.1126/science.1226191] [PMID: 23042294]
[44]
Wu PH, Isaji M, Carthew RW. Functionally diverse microRNA effector complexes are regulated by extracellular signaling. Mol Cell 2013; 52(1): 113-23.
[http://dx.doi.org/10.1016/j.molcel.2013.08.023] [PMID: 24055343]
[45]
Su S-F, Chang Y-W, Andreu-Vieyra C, et al. miR-30d, miR-181a and miR-199a-5p cooperatively suppress the endoplasmic reticulum chaperone and signaling regulator GRP78 in cancer. Oncogene 2013; 32(39): 4694-701.
[http://dx.doi.org/10.1038/onc.2012.483] [PMID: 23085757]
[46]
Dai B-H, Geng L, Wang Y, et al. microRNA-199a-5p protects hepatocytes from bile acid-induced sustained endoplasmic reticulum stress. Cell Death Dis 2013; 4(4): e604.
[http://dx.doi.org/10.1038/cddis.2013.134] [PMID: 23598416]
[47]
Barrey E, Saint-Auret G, Bonnamy B, Damas D, Boyer O, Gidrol X. Pre-microRNA and mature microRNA in human mitochondria. PLoS One 2011; 6(5): e20220.
[http://dx.doi.org/10.1371/journal.pone.0020220] [PMID: 21637849]
[48]
Wang G, Chen HW, Oktay Y, et al. PNPASE regulates RNA import into mitochondria. Cell 2010; 142(3): 456-67.
[http://dx.doi.org/10.1016/j.cell.2010.06.035] [PMID: 20691904]
[49]
Wang WX, Visavadiya NP, Pandya JD, Nelson PT, Sullivan PG, Springer JE. Mitochondria-associated microRNAs in rat hippocampus following traumatic brain injury. Exp Neurol 2015; 265: 84-93.
[http://dx.doi.org/10.1016/j.expneurol.2014.12.018] [PMID: 25562527]
[50]
Bandiera S, Rüberg S, Girard M, et al. Nuclear outsourcing of RNA interference components to human mitochondria. PLoS One 2011; 6(6): e20746.
[http://dx.doi.org/10.1371/journal.pone.0020746] [PMID: 21695135]
[51]
Zhang X, Zuo X, Yang B, et al. MicroRNA directly enhances mitochondrial translation during muscle differentiation. Cell 2014; 158(3): 607-19.
[http://dx.doi.org/10.1016/j.cell.2014.05.047] [PMID: 25083871]
[52]
Das S, Ferlito M, Kent OA, et al. Nuclear miRNA regulates the mitochondrial genome in the heart. Circ Res 2012; 110(12): 1596-603.
[http://dx.doi.org/10.1161/CIRCRESAHA.112.267732] [PMID: 22518031]
[53]
Fan S, Tian T, Chen W, et al. Mitochondrial miRNA determines chemoresistance by reprogramming metabolism and regulating mitochondrial transcription. Cancer Res 2019; 79(6): 1069-84.
[http://dx.doi.org/10.1158/0008-5472.CAN-18-2505] [PMID: 30659020]
[54]
Yan K, An T, Zhai M, et al. Mitochondrial miR-762 regulates apoptosis and myocardial infarction by impairing ND2. Cell Death Dis 2019; 10(7): 500.
[http://dx.doi.org/10.1038/s41419-019-1734-7] [PMID: 31235686]
[55]
Sripada L, Tomar D, Prajapati P, Singh R, Singh AK, Singh RS. Systematic analysis of small RNAs associated with human mitochondria by deep sequencing: detailed analysis of mitochondrial associated miRNA. PLoS One 2012; 7(9): e44873.
[http://dx.doi.org/10.1371/journal.pone.0044873]
[56]
Kren BT, Wong PYP, Sarver A, Zhang X, Zeng Y, Steer CJ. MicroRNAs identified in highly purified liver-derived mitochondria may play a role in apoptosis. RNA Biol 2009; 6(1): 65-72.
[http://dx.doi.org/10.4161/rna.6.1.7534] [PMID: 19106625]
[57]
Das S, Bedja D, Campbell N, et al. miR-181c regulates the mitochondrial genome, bioenergetics, and propensity for heart failure in vivo. PLoS One 2014; 9(5): e96820.
[http://dx.doi.org/10.1371/journal.pone.0096820] [PMID: 24810628]
[58]
Shepherd DL, Hathaway QA, Pinti MV, et al. Exploring the mitochondrial microRNA import pathway through Polynucleotide Phosphorylase (PNPase). J Mol Cell Cardiol 2017; 110: 15-25.
[http://dx.doi.org/10.1016/j.yjmcc.2017.06.012] [PMID: 28709769]
[59]
Wang X, Song C, Zhou X, Han X, Li J, Wang Z, et al. Mitochondria associated MicroRNA expression profiling of heart failure. Biomed Res Int 2017; 2017: 4042509.
[http://dx.doi.org/10.1155/2017/4042509]
[60]
Valadi H, Ekström K, Bossios A, Sjöstrand M, Lee JJ, Lötvall JO. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 2007; 9(6): 654-9.
[http://dx.doi.org/10.1038/ncb1596] [PMID: 17486113]
[61]
Gibbings DJ, Ciaudo C, Erhardt M, Voinnet O. Multivesicular bodies associate with components of miRNA effector complexes and modulate miRNA activity. Nat Cell Biol 2009; 11(9): 1143-9.
[http://dx.doi.org/10.1038/ncb1929] [PMID: 19684575]
[62]
Raiborg C, Stenmark H. The ESCRT machinery in endosomal sorting of ubiquitylated membrane proteins. Nature 2009; 458(7237): 445-52.
[http://dx.doi.org/10.1038/nature07961] [PMID: 19325624]
[63]
Vasquez-Rifo A, Bossé GD, Rondeau EL, Jannot G, Dallaire A, Simard MJ. A new role for the GARP complex in microRNA-mediated gene regulation. PLoS Genet 2013; 9(11): e1003961.
[http://dx.doi.org/10.1371/journal.pgen.1003961] [PMID: 24244204]
[64]
Kim YJ, Maizel A, Chen X. Traffic into silence: Endomembranes and post-transcriptional RNA silencing. EMBO J 2014; 33(9): 968-80.
[http://dx.doi.org/10.1002/embj.201387262] [PMID: 24668229]
[65]
Bose M, Barman B, Goswami A, Bhattacharyya SN. Spatiotemporal uncoupling of MicroRNA-mediated translational repression and target RNA degradation controls MicroRNP recycling in mammalian cells. Mol Cell Biol 2017; 37(4): e00464-16.
[http://dx.doi.org/10.1128/MCB.00464-16] [PMID: 27895152]
[66]
Lee YS, Pressman S, Andress AP, et al. Silencing by small RNAs is linked to endosomal trafficking. Nat Cell Biol 2009; 11(9): 1150-6.
[http://dx.doi.org/10.1038/ncb1930] [PMID: 19684574]
[67]
Hu P, Wang K, Zhou D, et al. GOLPH3 regulates exosome miRNA secretion in glioma cells. J Mol Neurosci 2020; 70(8): 1257-66.
[http://dx.doi.org/10.1007/s12031-020-01535-6] [PMID: 32227282]
[68]
Li H, Meng F, Ma J, et al. Insulin receptor substrate-1 and Golgi phosphoprotein 3 are downstream targets of miR-126 in esophageal squamous cell carcinoma. Oncol Rep 2014; 32(3): 1225-33.
[http://dx.doi.org/10.3892/or.2014.3327] [PMID: 25017784]
[69]
Liu Y, Sun Y, Zhao A. MicroRNA-134 suppresses cell proliferation in gastric cancer cells via targeting of GOLPH3. Oncol Rep 2017; 37(4): 2441-8.
[http://dx.doi.org/10.3892/or.2017.5488] [PMID: 28260021]
[70]
Zhang W, Chen X, Jia J. MiR-3150b-3p inhibits the progression of colorectal cancer cells via targeting GOLPH3. J Investig Med 2020; 68(2): 425-9.
[http://dx.doi.org/10.1136/jim-2019-001124] [PMID: 31678970]
[71]
Núñez-Olvera SI, Chávez-Munguía B, del Rocío Terrones-Gurrola MC, et al. A novel protective role for microRNA-3135b in Golgi apparatus fragmentation induced by chemotherapy via GOLPH3/AKT1/mTOR axis in colorectal cancer cells. Sci Rep 2020; 10(1): 10555.
[http://dx.doi.org/10.1038/s41598-020-67550-0] [PMID: 32601379]
[72]
Gagnon KT, Li L, Chu Y, Janowski BA, Corey DR. RNAi factors are present and active in human cell nuclei. Cell Rep 2014; 6(1): 211-21.
[http://dx.doi.org/10.1016/j.celrep.2013.12.013] [PMID: 24388755]
[73]
Schraivogel D, Schindler SG, Danner J, et al. Importin-β facilitates nuclear import of human GW proteins and balances cytoplasmic gene silencing protein levels. Nucleic Acids Res 2015; 43(15): 7447-61.
[http://dx.doi.org/10.1093/nar/gkv705] [PMID: 26170235]
[74]
Sarshad AA, Juan AH, Muler AIC, et al. Argonaute-miRNA complexes silence target mrnas in the nucleus of mammalian stem cells. Mol Cell 2018; 71(6): 1040-1050.e8.
[http://dx.doi.org/10.1016/j.molcel.2018.07.020] [PMID: 30146314]
[75]
Nishi K, Nishi A, Nagasawa T, Ui-Tei K. Human TNRC6A is an argonaute-navigator protein for microRNA-mediated gene silencing in the nucleus. RNA 2013; 19(1): 17-35.
[http://dx.doi.org/10.1261/rna.034769.112] [PMID: 23150874]
[76]
Weinmann L, Höck J, Ivacevic T, et al. Importin 8 is a gene silencing factor that targets argonaute proteins to distinct mRNAs. Cell 2009; 136(3): 496-507.
[http://dx.doi.org/10.1016/j.cell.2008.12.023] [PMID: 19167051]
[77]
Meister G, Landthaler M, Patkaniowska A, Dorsett Y, Teng G, Tuschl T. Human Argonaute2 mediates RNA cleavage targeted by miRNAs and siRNAs. Mol Cell 2004; 15(2): 185-97.
[http://dx.doi.org/10.1016/j.molcel.2004.07.007] [PMID: 15260970]
[78]
Hwang HW, Wentzel EA, Mendell JT. A hexanucleotide element directs microRNA nuclear import. Science 2007; 315(5808): 97-100.
[http://dx.doi.org/10.1126/science.1136235]
[79]
Park CW, Zeng Y, Zhang X, Subramanian S, Steer CJ. Mature microRNAs identified in highly purified nuclei from HCT116 colon cancer cells. RNA Biol 2010; 7(5): 606-14.
[http://dx.doi.org/10.4161/rna.7.5.13215] [PMID: 20864815]
[80]
Liao JY, Ma LM, Guo YH, et al. Deep sequencing of human nuclear and cytoplasmic small RNAs reveals an unexpectedly complex subcellular distribution of miRNAs and tRNA 3′ trailers. PLoS One 2010; 5(5): e10563.
[http://dx.doi.org/10.1371/journal.pone.0010563] [PMID: 20498841]
[81]
Chatterjee S, Großhans H. Active turnover modulates mature microRNA activity in Caenorhabditis elegans. Nature 2009; 461(7263): 546-9.
[http://dx.doi.org/10.1038/nature08349] [PMID: 19734881]
[82]
Turunen TA, Roberts TC, Laitinen P, et al. Changes in nuclear and cytoplasmic microRNA distribution in response to hypoxic stress. Sci Rep 2019; 9(1): 10332.
[http://dx.doi.org/10.1038/s41598-019-46841-1] [PMID: 31316122]
[83]
Zaratiegui M, Castel SE, Irvine DV, et al. RNAi promotes heterochromatic silencing through replication-coupled release of RNA Pol II. Nature 2011; 479(7371): 135-8.
[http://dx.doi.org/10.1038/nature10501] [PMID: 22002604]
[84]
Ameyar-Zazoua M, Rachez C, Souidi M, et al. Argonaute proteins couple chromatin silencing to alternative splicing. Nat Struct Mol Biol 2012; 19(10): 998-1004.
[http://dx.doi.org/10.1038/nsmb.2373] [PMID: 22961379]
[85]
Leucci E, Patella F, Waage J, et al. microRNA-9 targets the long non-coding RNA MALAT1 for degradation in the nucleus. Sci Rep 2013; 3(1): 2535.
[http://dx.doi.org/10.1038/srep02535] [PMID: 23985560]
[86]
Fasanaro P, Greco S, Lorenzi M, et al. An integrated approach for experimental target identification of hypoxia-induced miR-210. J Biol Chem 2009; 284(50): 35134-43.
[http://dx.doi.org/10.1074/jbc.M109.052779] [PMID: 19826008]
[87]
Hansen TB, Wiklund ED, Bramsen JB, et al. miRNA-dependent gene silencing involving Ago2-mediated cleavage of a circular antisense RNA. EMBO J 2011; 30(21): 4414-22.
[http://dx.doi.org/10.1038/emboj.2011.359] [PMID: 21964070]
[88]
Tang R, Li L, Zhu D, et al. Mouse miRNA-709 directly regulates miRNA-15a/16-1 biogenesis at the posttranscriptional level in the nucleus: evidence for a microRNA hierarchy system. Cell Res 2012; 22(3): 504-15.
[http://dx.doi.org/10.1038/cr.2011.137] [PMID: 21862971]
[89]
Zisoulis DG, Kai ZS, Chang RK, Pasquinelli AE. Autoregulation of microRNA biogenesis by let-7 and Argonaute. Nature 2012; 486(7404): 541-4.
[http://dx.doi.org/10.1038/nature11134] [PMID: 22722835]
[90]
Hicks JA, Li L, Matsui M, et al. Human GW182 paralogs are the central organizers for RNA-mediated control of transcription. Cell Rep 2017; 20(7): 1543-52.
[http://dx.doi.org/10.1016/j.celrep.2017.07.058] [PMID: 28813667]
[91]
Verdel A, Jia S, Gerber S, Sugiyama T, Gygi S, Grewal SI MD. RNAi-mediated targeting of heterochromatin by the RITS complex. Science 2004; 303(5658): 672-6.
[http://dx.doi.org/10.1126/science.1093686]
[92]
Abernathy DG, Kim WK, McCoy MJ, et al. MicroRNAs induce a permissive chromatin environment that enables neuronal subtype-specific reprogramming of adult human fibroblasts. Cell Stem Cell 2017; 21(3): 332-348.e9.
[http://dx.doi.org/10.1016/j.stem.2017.08.002] [PMID: 28886366]
[93]
Krivdova G, Erwin SE, Voisin V, et al. Microrna-130a regulates hematopoietic stem cell self-renewal by repressing chromatin modifiers and shaping the accessible chromatin landscape. Blood 2018; 132(S1): 3824-4.
[http://dx.doi.org/10.1182/blood-2018-99-116866]
[94]
Ritland Politz JC, Zhang F, Pederson T. MicroRNA-206 colocalizes with ribosome-rich regions in both the nucleolus and cytoplasm of rat myogenic cells. Proc Natl Acad Sci 2006; 103(50): 18957-62.
[http://dx.doi.org/10.1073/pnas.0609466103] [PMID: 17135348]
[95]
Ritland Politz JC, Hogan EM, Pederson T. MicroRNAs with a nucleolar location. RNA 2009; 15(9): 1705-15.
[http://dx.doi.org/10.1261/rna.1470409] [PMID: 19628621]
[96]
Li ZF, Liang YM, Lau PN, et al. Dynamic localisation of mature microRNAs in Human nucleoli is influenced by exogenous genetic materials. PLoS One 2013; 8(8): e70869.
[http://dx.doi.org/10.1371/journal.pone.0070869] [PMID: 23940654]
[97]
Bai B, Liu H, Laiho M. Small RNA expression and deep sequencing analyses of the nucleolus reveal the presence of nucleolus-associated microRNAs. FEBS Open Biol 2014; 4(1): 441-9.
[http://dx.doi.org/10.1016/j.fob.2014.04.010] [PMID: 24918059]
[98]
Atwood BL, Woolnough JL, Lefevre GM, Saint Just Ribeiro M, Felsenfeld G, Giles KE. Human argonaute 2 is tethered to ribosomal RNA through MicroRNA interactions. J Biol Chem 2016; 291(34): 17919-28.
[http://dx.doi.org/10.1074/jbc.M116.725051] [PMID: 27288410]
[99]
Pisani G, Baron B. Nuclear paraspeckles function in mediating gene regulatory and apoptotic pathways. Noncoding RNA Res 2019; 4(4): 128-34.
[http://dx.doi.org/10.1016/j.ncrna.2019.11.002] [PMID: 32072080]
[100]
Jiang L, Shao C, Wu QJ, et al. NEAT1 scaffolds RNA-binding proteins and the Microprocessor to globally enhance pri-miRNA processing. Nat Struct Mol Biol 2017; 24(10): 816-24.
[http://dx.doi.org/10.1038/nsmb.3455] [PMID: 28846091]
[101]
West JA, Davis CP, Sunwoo H, et al. The long noncoding RNAs NEAT1 and MALAT1 bind active chromatin sites. Mol Cell 2014; 55(5): 791-802.
[http://dx.doi.org/10.1016/j.molcel.2014.07.012] [PMID: 25155612]
[102]
Nakagawa S, Naganuma T, Shioi G, Hirose T. Paraspeckles are subpopulation-specific nuclear bodies that are not essential in mice. J Cell Biol 2011; 193(1): 31-9.
[http://dx.doi.org/10.1083/jcb.201011110] [PMID: 21444682]
[103]
Yan H, Wang Z, Sun Y, Hu L, Bu P. Cytoplasmic NEAT1 suppresses AML stem cell self‐renewal and leukemogenesis through inactivation of Wnt signaling. Adv Sci 2021; 8(22): 2100914.
[http://dx.doi.org/10.1002/advs.202100914] [PMID: 34609794]
[104]
Liang J, Liu C, Xu D, Xie K, Li A. LncRNA NEAT1 facilitates glioma progression via stabilizing PGK1. J Transl Med 2022; 20(1): 80.
[http://dx.doi.org/10.1186/s12967-022-03273-2] [PMID: 35123484]
[105]
Turchinovich A, Samatov TR, Tonevitsky AGBB, Burwinkel B. Circulating miRNAs: cell-cell communication function? Front Genet 2013; 4(119): 119.
[PMID: 23825476]
[106]
Ono M, Kosaka N, Tominaga N, et al. Exosomes from bone marrow mesenchymal stem cells contain a microRNA that promotes dormancy in metastatic breast cancer cells. Sci Signal 2014; 7(332): ra63.
[http://dx.doi.org/10.1126/scisignal.2005231] [PMID: 24985346]
[107]
Mori MA, Ludwig RG, Garcia-Martin R, Brandão BB, Kahn CR. Extracellular miRNAs: From Biomarkers to Mediators of Physiology and Disease. Cell Metab 2019; 30(4): 656-73.
[http://dx.doi.org/10.1016/j.cmet.2019.07.011] [PMID: 31447320]
[108]
Thomou T, Mori MA, Dreyfuss JM, et al. Adipose-derived circulating miRNAs regulate gene expression in other tissues. Nature 2017; 542(7642): 450-5.
[http://dx.doi.org/10.1038/nature21365] [PMID: 28199304]
[109]
Castaño C, Kalko S, Novials A, Párrizas M. Obesity-associated exosomal miRNAs modulate glucose and lipid metabolism in mice. Proc Natl Acad Sci 2018; 115(48): 12158-63.
[http://dx.doi.org/10.1073/pnas.1808855115] [PMID: 30429322]
[110]
Wang R, Hong J, Cao Y, et al. Elevated circulating microRNA-122 is associated with obesity and insulin resistance in young adults. Eur J Endocrinol 2015; 172(3): 291-300.
[http://dx.doi.org/10.1530/EJE-14-0867] [PMID: 25515554]
[111]
Willeit P, Skroblin P, Moschen AR, et al. Circulating MicroRNA-122 is associated with the risk of new-onset metabolic syndrome and type 2 diabetes. Diabetes 2017; 66(2): 347-57.
[http://dx.doi.org/10.2337/db16-0731] [PMID: 27899485]
[112]
Vickers KC, Palmisano BT, Shoucri BM, Shamburek RD, Remaley AT. MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins. Nat Cell Biol 2011; 13(4): 423-33.
[http://dx.doi.org/10.1038/ncb2210] [PMID: 21423178]
[113]
Zhang A, Li D, Liu Y, Li J, Zhang Y, Zhang CY. Islet β cell: An endocrine cell secreting miRNAs. Biochem Biophys Res Commun 2018; 495(2): 1648-54.
[http://dx.doi.org/10.1016/j.bbrc.2017.12.028] [PMID: 29223394]
[114]
Lee HK, Finniss S, Cazacu S, Xiang C, Brodie C. Mesenchymal stem cells deliver exogenous miRNAs to neural cells and induce their differentiation and glutamate transporter expression. Stem Cells Dev 2014; 23(23): 2851-61.
[http://dx.doi.org/10.1089/scd.2014.0146] [PMID: 25036385]
[115]
Manca S, Upadhyaya B, Mutai E, et al. Milk exosomes are bioavailable and distinct microRNA cargos have unique tissue distribution patterns. Sci Rep 2018; 8(1): 11321.
[http://dx.doi.org/10.1038/s41598-018-29780-1] [PMID: 30054561]
[116]
Kosaka N, Izumi H, Sekine K, Ochiya T. microRNA as a new immune-regulatory agent in breast milk. Silence 2010; 1(1): 7.
[http://dx.doi.org/10.1186/1758-907X-1-7] [PMID: 20226005]
[117]
Tsukamoto M, Iinuma H, Yagi T, Matsuda K, Hashiguchi Y. Circulating exosomal MicroRNA-21 as a biomarker in each tumor stage of colorectal cancer. Oncology 2017; 92(6): 360-70.
[http://dx.doi.org/10.1159/000463387] [PMID: 28376502]
[118]
Wang H, Peng R, Wang J, Qin Z, Xue L. Circulating microRNAs as potential cancer biomarkers: the advantage and disadvantage. Clin Epigenet 2018; 10(1): 59.
[http://dx.doi.org/10.1186/s13148-018-0492-1] [PMID: 29713393]
[119]
Arroyo JD, Chevillet JR, Kroh EM, et al. Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc Natl Acad Sci 2011; 108(12): 5003-8.
[http://dx.doi.org/10.1073/pnas.1019055108] [PMID: 21383194]
[120]
Wang K, Zhang S, Weber J, Baxter D, Galas DJ. Export of microRNAs and microRNA-protective protein by mammalian cells. Nucleic Acids Res 2010; 38(20): 7248-59.
[http://dx.doi.org/10.1093/nar/gkq601] [PMID: 20615901]
[121]
Shimizu C, Kim J, Stepanowsky P, et al. Differential expression of miR-145 in children with Kawasaki disease. PLoS One 2013; 8(3): e58159.
[http://dx.doi.org/10.1371/journal.pone.0058159] [PMID: 23483985]
[122]
Tsai YW, Sung HH, Li JC, et al. Glia-derived exosomal miR-274 targets Sprouty in trachea and synaptic boutons to modulate growth and responses to hypoxia. Proc Natl Acad Sci 2019; 116(49): 24651-61.
[http://dx.doi.org/10.1073/pnas.1902537116] [PMID: 31666321]
[123]
Lawrie CH, Gal S, Dunlop HM, et al. Detection of elevated levels of tumour-associated microRNAs in serum of patients with diffuse large B-cell lymphoma. Br J Haematol 2008; 141(5): 672-5.
[http://dx.doi.org/10.1111/j.1365-2141.2008.07077.x] [PMID: 18318758]
[124]
Liu Q, Yu Z, Yuan S, et al. Circulating exosomal microRNAs as prognostic biomarkers for non-small-cell lung cancer. Oncotarget 2017; 8(8): 13048-58.
[http://dx.doi.org/10.18632/oncotarget.14369] [PMID: 28055956]
[125]
Rashad NM, Ateya MAM, Saraya YS, et al. Association of miRNA − 320 expression level and its target gene endothelin-1 with the susceptibility and clinical features of polycystic ovary syndrome. J Ovarian Res 2019; 12(1): 39.
[http://dx.doi.org/10.1186/s13048-019-0513-5]
[126]
Machida T, Tomofuji T, Maruyama T, et al. miR-1246 and miR-4644 in salivary exosome as potential biomarkers for pancreatobiliary tract cancer. Oncol Rep 2016; 36(4): 2375-81.
[http://dx.doi.org/10.3892/or.2016.5021] [PMID: 27573701]
[127]
Rabinowits G, Gerçel-Taylor C, Day JM, Taylor DD, Kloecker GH. Exosomal microRNA: A diagnostic marker for lung cancer. Clin Lung Cancer 2009; 10(1): 42-6.
[http://dx.doi.org/10.3816/CLC.2009.n.006] [PMID: 19289371]
[128]
Taylor DD, Gercel-Taylor C. MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer. Gynecol Oncol 2008; 110(1): 13-21.
[http://dx.doi.org/10.1016/j.ygyno.2008.04.033] [PMID: 18589210]
[129]
Yang TT, Liu CG, Gao SC, Zhang Y, Wang PC. The serum exosome derived MicroRNA-135a, -193b, and -384 were potential Alzheimer’s disease biomarkers. Biomed Environ Sci 2018; 31(2): 87-96.
[PMID: 29606187]
[130]
Gui Y, Liu H, Zhang L, Lv W, Hu X. Altered microRNA profiles in cerebrospinal fluid exosome in Parkinson disease and Alzheimer disease. Oncotarget 2015; 6(35): 37043-53.
[http://dx.doi.org/10.18632/oncotarget.6158] [PMID: 26497684]
[131]
Wang GK, Zhu JQ, Zhang JT, et al. Circulating microRNA: A novel potential biomarker for early diagnosis of acute myocardial infarction in humans. Eur Heart J 2010; 31(6): 659-66.
[http://dx.doi.org/10.1093/eurheartj/ehq013] [PMID: 20159880]
[132]
Eichelser C, Stückrath I, Müller V, et al. Increased serum levels of circulating exosomal microRNA-373 in receptor-negative breast cancer patients. Oncotarget 2014; 5(20): 9650-63.
[http://dx.doi.org/10.18632/oncotarget.2520] [PMID: 25333260]
[133]
Sueta A, Yamamoto Y, Iwase H. The role of exosomal microRNAs; focus on clinical applications in breast cancer. Cancer Drug Resist 2019; 2(3): 847-61.
[http://dx.doi.org/10.20517/cdr.2019.17] [PMID: 35582569]
[134]
Herwijnen MJC, Driedonks TAP, Snoek BL, et al. Abundantly present miRNAs in milk-derived extracellular vesicles are conserved between mammals. Front Nutr 2018; 5: 81.
[http://dx.doi.org/10.3389/fnut.2018.00081] [PMID: 30280098]
[135]
Vizitiu AC, Stambouli D, Pavel AG, et al. Mature miR-99a upregulation in the amniotic fluid samples from female fetus down syndrome pregnancies: A pilot study. MedM 2019; 55(11)
[http://dx.doi.org/10.3390/medicina55110728]
[136]
Hicks SD, Carpenter RL, Wagner KE, et al. Saliva MicroRNA differentiates children with autism from peers with typical and atypical development. J Am Acad Child Adolesc Psychiatry 2020; 59(2): 296-308.
[http://dx.doi.org/10.1016/j.jaac.2019.03.017] [PMID: 30926572]
[137]
Wiegand C, Heusser P, Klinger C, et al. Stress-associated changes in salivary microRNAs can be detected in response to the Trier Social Stress Test: An exploratory study. Sci Rep 2018; 8(1): 7112.
[http://dx.doi.org/10.1038/s41598-018-25554-x] [PMID: 29740073]
[138]
Muñoz-San Martín M, Reverter G, Robles-Cedeño R, et al. Analysis of miRNA signatures in CSF identifies upregulation of miR-21 and miR-146a/b in patients with multiple sclerosis and active lesions. J Neuroinflammation 2019; 16(1): 220.
[http://dx.doi.org/10.1186/s12974-019-1590-5] [PMID: 31727077]
[139]
Kopkova A, Sana J, Fadrus P, Slaby O. Cerebrospinal fluid microRNAs as diagnostic biomarkers in brain tumors. Clinical Chemistry and Laboratory Medicine (CCLM) 2018; 56(6): 869-79.
[http://dx.doi.org/10.1515/cclm-2017-0958] [PMID: 29451858]
[140]
Zardo G, Ciolfi A, vian L. Polycombs and microRNA-223 regulate human granulopoiesis by transcriptional control of target gene expression. (Blood (2012) 119, 17, (4034-4046)). Blood 2014; 123(8): 1279.
[http://dx.doi.org/10.1182/blood-2014-01-548255]
[141]
Wang D, Sun X, Wei Y, et al. Nuclear miR-122 directly regulates the biogenesis of cell survival oncomiR miR-21 at the posttranscriptional level. Nucleic Acids Res 2018; 46(4): 2012-29.
[http://dx.doi.org/10.1093/nar/gkx1254] [PMID: 29253196]
[142]
Zhang WL, Zhang JH. miR-181c promotes proliferation via suppressing PTEN expression in inflammatory breast cancer. Int J Oncol 2015; 46(5): 2011-20.
[http://dx.doi.org/10.3892/ijo.2015.2896] [PMID: 25695913]
[143]
Ristori E, Lopez-Ramirez MA, Narayanan A, et al. A Dicer-miR-107 interaction regulates biogenesis of specific miRNAs crucial for neurogenesis. Dev Cell 2015; 32(5): 546-60.
[http://dx.doi.org/10.1016/j.devcel.2014.12.013] [PMID: 25662174]
[144]
Bonev B, Pisco A, Papalopulu N. MicroRNA-9 reveals regional diversity of neural progenitors along the anterior-posterior axis. Dev Cell 2011; 20(1): 19-32.
[http://dx.doi.org/10.1016/j.devcel.2010.11.018] [PMID: 21238922]
[145]
Ryan DG, Oliveira-Fernandes M, Lavker RM. MicroRNAs of the mammalian eye display distinct and overlapping tissue specificity. Mol Vis 2006; 12: 1175-84.
[PMID: 17102797]
[146]
Yu J, Ryan DG, Getsios S, Oliveira-Fernandes M, Fatima A, Lavker RM. MicroRNA-184 antagonizes microRNA-205 to maintain SHIP2 levels in epithelia. Proc Natl Acad Sci 2008; 105(49): 19300-5.
[http://dx.doi.org/10.1073/pnas.0803992105] [PMID: 19033458]
[147]
Pase L, Layton JE, Kloosterman WP, Carradice D, Waterhouse PM, Lieschke GJ. miR-451 regulates zebrafish erythroid maturation in vivo via its target gata2. Blood 2009; 113(8): 1794-804.
[http://dx.doi.org/10.1182/blood-2008-05-155812] [PMID: 18849488]
[148]
Yu D, dos Santos CO, Zhao G, et al. miR-451 protects against erythroid oxidant stress by repressing 14-3-3ζ. Genes Dev 2010; 24(15): 1620-33.
[http://dx.doi.org/10.1101/gad.1942110] [PMID: 20679398]
[149]
Tsuchiya S, Oku M, Imanaka Y, et al. MicroRNA-338-3p and microRNA-451 contribute to the formation of basolateral polarity in epithelial cells. Nucleic Acids Res 2009; 37(11): 3821-7.
[http://dx.doi.org/10.1093/nar/gkp255] [PMID: 19386621]
[150]
Labbaye C, Spinello I, Quaranta MT, et al. A three-step pathway comprising PLZF/miR-146a/CXCR4 controls megakaryopoiesis. Nat Cell Biol 2008; 10(7): 788-801.
[http://dx.doi.org/10.1038/ncb1741] [PMID: 18568019]
[151]
Nguyen LS, Fregeac J, Bole-Feysot C, et al. Role of miR-146a in neural stem cell differentiation and neural lineage determination: relevance for neurodevelopmental disorders. Mol Autism 2018; 9(1): 38.
[http://dx.doi.org/10.1186/s13229-018-0219-3] [PMID: 29951184]
[152]
Bagga S, Bracht J, Hunter S, et al. Regulation by let-7 and lin-4 miRNAs Results in Target mRNA Degradation. Cell 2005; 122(4): 553-63.
[http://dx.doi.org/10.1016/j.cell.2005.07.031] [PMID: 16122423]
[153]
Großhans H, Johnson T, Reinert KL, Gerstein M, Slack FJ. The temporal patterning microRNA let-7 regulates several transcription factors at the larval to adult transition in C. elegans. Dev Cell 2005; 8(3): 321-30.
[http://dx.doi.org/10.1016/j.devcel.2004.12.019] [PMID: 15737928]
[154]
Van Wynsberghe PM, Kai ZS, Massirer KB, Burton VH, Yeo GW, Pasquinelli AE. LIN-28 co-transcriptionally binds primary let-7 to regulate miRNA maturation in Caenorhabditis elegans. Nat Struct Mol Biol 2011; 18(3): 302-8.
[http://dx.doi.org/10.1038/nsmb.1986] [PMID: 21297634]
[155]
Borzi C, Calzolari L, Centonze G, Milione M, Sozzi G, Fortunato O. mir-660-p53-mir-486 network: A new key regulatory pathway in lung tumorigenesis. Int J Mol Sci 2017; 18(1): 222.
[http://dx.doi.org/10.3390/ijms18010222] [PMID: 28124991]
[156]
O’Connell RM, Rao DS, Chaudhuri AA, et al. Sustained expression of microRNA-155 in hematopoietic stem cells causes a myeloproliferative disorder. J Exp Med 2008; 205(3): 585-94.
[http://dx.doi.org/10.1084/jem.20072108] [PMID: 18299402]
[157]
Fukao T, Fukuda Y, Kiga K, et al. An evolutionarily conserved mechanism for microRNA-223 expression revealed by microRNA gene profiling. Cell 2007; 129(3): 617-31.
[http://dx.doi.org/10.1016/j.cell.2007.02.048] [PMID: 17482553]
[158]
Pulikkan JA, Dengler V, Peramangalam PS, et al. Cell-cycle regulator E2F1 and microRNA-223 comprise an autoregulatory negative feedback loop in acute myeloid leukemia. Blood 2010; 115(9): 1768-78.
[http://dx.doi.org/10.1182/blood-2009-08-240101] [PMID: 20029046]
[159]
Li T, Morgan MJ, Choksi S, Zhang Y, Kim YS, Liu Z. MicroRNAs modulate the noncanonical transcription factor NF-κB pathway by regulating expression of the kinase IKKα during macrophage differentiation. Nat Immunol 2010; 11(9): 799-805.
[http://dx.doi.org/10.1038/ni.1918] [PMID: 20711193]
[160]
Eiring AM, Harb JG, Neviani P, et al. miR-328 functions as an RNA decoy to modulate hnRNP E2 regulation of mRNA translation in leukemic blasts. Cell 2010; 140(5): 652-65.
[http://dx.doi.org/10.1016/j.cell.2010.01.007] [PMID: 20211135]
[161]
Pulikkan JA, Peramangalam PS, Dengler V, et al. C/EBPα regulated microRNA-34a targets E2F3 during granulopoiesis and is down-regulated in AML with CEBPA mutations. Blood 2010; 116(25): 5638-49.
[http://dx.doi.org/10.1182/blood-2010-04-281600] [PMID: 20889924]

Rights & Permissions Print Cite
Article Metrics
25
2
Wayfinder Image
Open Access Journals Promotions
© 2024 Bentham Science Publishers | Privacy Policy